Relationship of Negative Contrast to Animal Models of Fear and Anxiety

Animal Learning & Behavior /998,26 (4),397-407 Relationship ofnegative contrast to animal models offear and anxiety CHARLES F,FLAHERTY, ANNAGREENWOOD, JOSEPH MARTIN, and MARY LESZCZUK Rutgers University, Piscataway, New Jersey The relatedness of behavior elicited by reward reduction (successive negative contrast procedure) and behaviors produced by three animal models of anxiety (open-field emergence, elevated plus-maze, and context-shock fear conditioning) was examined by correlational and factor analytic procedures, Factor analysis (oblique rotation) indicated substantial independence among the tests: Trials 1 and 2 of the plus-maze loaded on two different factors unaccompanied by any other test; open-field emer gence and context-shock fear loaded on the same factor; and negative contrast loaded on a fourth fac tor. However, negative contrast proved to be a dynamic process, with factor loadings changing across a 4-day postshift period-moving from an independent loading on the 1st postshift day to being clus tered with context-shock fear and open-field emergence on the 2nd and 3rd postshift days to being clustered with just context-shock fear on the last postshift day. These latter datasupport a multistage theory ofsuccessive negative contrast. Rats shifted from a preferred reward to a less preferred We have recently proposed a multistage theory ofSNC reward show an abrupt decrement in goal-directed behav that suggests that perceptual and cognitive stages (detec ior and an increase in exploratory behavior (e.g., Crespi, tion that the new reward is different from the memory of 1942, 1944; Elliott, 1928; Flaherty, 1996). The goal the preshift reward; hedonic evaluation ofthe new reward; directed performance of the shifted rats decreases to a search for the "missing" reward if the new reward is of level below that of unshifted control animals given the lesser value) precede the activation of an emotional re same level of reward-an outcome termed a successive sponse to reward reduction (Flaherty, 1996). In the present negative contrast (SNC) effect. paper, we are concerned with an investigation ofthis hy One enduring interpretation of successive negative pothesis, and we compare daily postshift performance of contrast is that it is caused by an emotional reaction to the rats downshifted in reward with their performance in three reward reduction. Terms such as anger, depression, dis procedures frequently used to assess anxiety or fear in rats: appointment, andfrustration have often been used in re the elevated plus-maze, context-shock fear conditioning, ferring to a rat's or a monkey's reaction to reduced reward and emergence from the home cage to an open field. ie.g., Amsel, 1992; Crespi, 1942, 1944; Flaherty, Krauss, Correlational and factor analytic approaches to animal Rowan, & Grigson, 1994; Gray, 1982, 1987; Spence, models ofanxiety have been used in a number of recent 1956), Evidence supporting the involvement of some papers. Belzung and Le Pape (1994) examined the cor form ofstress in negative contrast includes the success of relations in behavior among five different novelty related antianxiety agents (e.g., benzodiazepines, ethanol, bar tests: light/dark choice, elevated plus-maze, holeboard, biturates, and morphine) in alleviating aspects ofcontrast free exposure to a novel space, and confrontation with a (Becker & Flaherty, 1982; Flaherty, 1991b, 1996), the el novel object. The authors concluded the five different tests evation ofcorticosteroids as a consequence ofreward re ofnovelty induced anxiety were not measuring the same duction (Flaherty, Becker, & Pohorecky, 1985; Goldman, psychological state. In a factor analytic study ofdefensive Coover, & Levine, 1973; Mitchell & Flaherty, 1998), co behaviors in mice, Griebel, Blanchard, and Blanchard variation of contrast and other forms ofemotional reac (1996) concluded that there were five different aspects of tivity in rats selectively bred for performance in avoid anxiety measured by their 17 variables. Other studies have ance learning (Flaherty & Rowan, 1989), and the role of also raised the issue that different tasks or test procedures amygdala lesions in reducing contrast (Becker, Jarvis, may be measuring different aspects ofanxiety (File, 1991, Wagner, & Flaherty, 1984). 1995; Handley, McBlane, Critchley, & Njung'e, 1993; Rodgers, Cole, Aboualfa, & Stephenson, 1995). In some cases, a single test may measure multiple components of This research was funded by NIH Grant MH48835 and by funds from anxiety. Exposure ofmice to a single 5-min trial in an el the Dean of Arts and SCIencesat Rutgers to the first author, The assis evated plus-maze may yield from two to six factors, de tance of Cynthia Coppotelli and Matthew Kelsey is greatly appreciated, pending on the number and nature ofdependent variables Correspondence should be addressed to C. F.Flaherty, Psychology De partment, New Brunswick campus, Rutgers University. 152 Freling scored (Rodgers & Johnson, 1995). However, the sub huysen Rd., Piscataway, NJ 08854-8020 (e-mail: tlaherty@psycho-b. stantial effectiveness ofthe benzodiazepine tranquilizers rutgers.edu). in many animal models ofanxiety suggests that there must 397 Copyright 1998 Psychonomic Society, Inc, 398 FLAHERTY, GREENWOOD, MARTIN, AND LESZCZUK also be some degree ofcommonality (Davis, 1991; Fla suppress open-arm entries (Handley et al., 1993; Pellow herty, 1991a, 1991b; Howard & Pollard, 1991; Lister, & File, 1986; Rodgers et aI., 1995). 1991). Behavior in a second trial in the elevated plus-maze In comparing negative contrast with other models of differs from that seen on the first trial. Benzodiazepines anxiety, we used a negative contrast procedure that in have been found to be ineffective in the second trial, re volved the consumption of sugar solutions. Rats were gardless of whether they were administered on the first given access to a 32% sucrose solution for 5 min a day trial, leading to the suggestion that the second trial mea for 10 days, and, on the 11th day, shifted to a 4% sucrose sures a different type ofanxiety than the first trial (File, solution. Typically, the "shifted" rats lick substantially 1990). This has been supported by factor analytic stud less ofthe 4% solution than do "unshifted" controls, but ies that found that the measures ofTrial 1 load on a dif the shifted rats recover from contrast after approximately ferent factor from those ofTrial 2 (e.g., Fernandes & File, 4 days of access to the new solution (Flaherty, Krauss, 1996; File, Zangrossi, Viana, & Graeff, 1993). Rowan, & Grigson, 1994). The involvement ofsome as Context-shock fear conditioning differs from the above pect ofanxiety or stress in negative contrast is indicated models in that it involves a physically aversive event. by the fact that corticosterone levels are elevated after Corticosterone levels have been shown to be elevated after the 2nd, but not the 1st, postshift day (Flaherty et aI., 1985; exposure to the context in which shocks had been given Mitchell & Flaherty, 1998) and that chlordiazepoxide (Urban, Van de Kar, Lorens, & Bethea, 1986), and benzo and ethanol reduce contrast when administered acutely diazepines disrupt conditioned fear (Fanselow & Helm on the 2nd postshift day, although they are not effective stetter, 1988; Sanger & Joly, 1985), whereas anxiogenics on the 1st postshift day (Flaherty, 1996; Flaherty, Grig enhance conditioned fear (Fanselow, Helmstetter, & Cal son, & Lind, 1990). cagnetti, 1991). The test battery selected for comparison with contrast The principal purpose of this experiment was to de in the present experiment included a measure ofnovelty termine whether behavior at different stages ofthe con induced anxiety (emergence from the home cage to an trast recovery cycle was differentially correlated with open field), conditioned fear (context-shock pairings), these tests. A secondary purpose was to determine the and a test that involved both generalized anxiety and a relatedness ofthe other three tests themselves. specific fear ofopen places (elevated plus-maze). Previ ous studies have investigated novelty-induced anxiety by METHOD measuring latency to emerge from a familiar area to an unfamiliar area (Corey, 1978; Hughes, 1968; Maren, Subjects Patel, Thompson, & Mitchell, 1993), such as from the Sixty male Sprague-Dawley rats purchased from Harlan were animal's cage to a table top (Henck, Mattsson, Rezabek, used as subjects. The rats were approximately 90 days old, weigh Carlson, & Rech, 1994), runway (King, 1968), or open ing 300-350 g at the beginning ofthe experiment. The animals were field (Jellestad, Markowska, Bakke, & Walther, 1986). individually housed under 14:lO-h light:dark conditions. The rats were given free access to water and were maintained at 82% oftheir The evidence that exposure to novel context induces anx free-fed weight by once-daily feedings. The deprivation regimen is iety in laboratory animals includes increased heart rate, standard for negative contrast experiments. increased defecation, and increased corticosterone release The rats were run in two consecutive groups of30 each, approx (Blanchard, Kelley, & Blanchard, 1974; Crawley, 1985; imately I h months apart. Thirty ofthe subjects were subsequently Misslin & Cigrang, 1986). In these tests, antianxiety drugs used in an anticipatory contrast study and then underwent fear con increase ambulation (Treit, 1985), increase exploration ditioning. The fear conditioning, but not the anticipatory contrast, data

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